Elevated performance: The unique physiology of birds that fly at high altitudes

Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4K1, Canada.
Journal of Experimental Biology (Impact Factor: 2.9). 08/2011; 214(Pt 15):2455-62. DOI: 10.1242/jeb.052548
Source: PubMed


Birds that fly at high altitudes must support vigorous exercise in oxygen-thin environments. Here I discuss the characteristics that help high fliers sustain the high rates of metabolism needed for flight at elevation. Many traits in the O(2) transport pathway distinguish birds in general from other vertebrates. These include enhanced gas-exchange efficiency in the lungs, maintenance of O(2) delivery and oxygenation in the brain during hypoxia, augmented O(2) diffusion capacity in peripheral tissues and a high aerobic capacity. These traits are not high-altitude adaptations, because they are also characteristic of lowland birds, but are nonetheless important for hypoxia tolerance and exercise capacity. However, unique specializations also appear to have arisen, presumably by high-altitude adaptation, at every step in the O(2) pathway of highland species. The distinctive features of high fliers include an enhanced hypoxic ventilatory response, an effective breathing pattern, larger lungs, haemoglobin with a higher O(2) affinity, further augmentation of O(2) diffusion capacity in the periphery and multiple alterations in the metabolic properties of cardiac and skeletal muscle. These unique specializations improve the uptake, circulation and efficient utilization of O(2) during high-altitude hypoxia. High-altitude birds also have larger wings than their lowland relatives to reduce the metabolic costs of staying aloft in low-density air. High fliers are therefore unique in many ways, but the relative roles of adaptation and plasticity (acclimatization) in high-altitude flight are still unclear. Disentangling these roles will be instrumental if we are to understand the physiological basis of altitudinal range limits and how they might shift in response to climate change.

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    • "An earlier, and seemingly overlooked, hypothesis posited that hypoxic exposure actually enhances aerobic bioenergetics (Hochachka et al., 1983). In line with this theory, animals that are consistently exposed to hypoxic conditions have evolved with measures of enhanced skeletal muscle oxidative capacity (Valdivia, 1958; Scott, 2011). The high altitude native barheaded goose has skeletal muscle mitochondria that appear redistributed closer to adjacent capillaries (Scott et al., 2009) and hypobaric hypoxia increased mitochondrial density in murine cerebral subcortex (Gutsaeva et al., 2008). "
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    ABSTRACT: The role of hypoxia on skeletal muscle mitochondria is controversial. Studies superimposing exercise training with hypoxic exposure demonstrate an increase in skeletal muscle mitochondrial volume density (MitoVD ) over equivalent normoxic training. In contrast, a reduction in both skeletal muscle mass and MitoVD have been reported following mountaineering expeditions. These observations may however be confounded by negative energy balance, which may obscure the results. Accordingly we sought to examine the effects of high altitude hypoxic exposure on mitochondrial characteristics, with emphasis on MitoVD , while minimizing changes in energy balance. For this purpose, skeletal muscle biopsies were obtained from 9 lowlanders at sea level (Pre) and following 7 (7 Days) and 28 (28 Days) days of exposure to 3454 m. Maximal ergometer power output, whole-body weight and composition, leg lean mass, and skeletal muscle fibre area all remained unchanged following the altitude exposure. Transmission electron microscopy determined intermyofibrillar (IMF) MitoVD was augmented (P = 0.028) by 11.5 ± 9.2% from Pre (5.05 ± 0.9%) to Day 28 (5.61 ± 0.04%). On the contrary, there was no change in subsarcolemmal (SS) MitoVD . As a result total MitoVD (IMF + SS) was increased (P = 0.031) from 6.20 ± 1.5% at Pre to 6.62 ± 1.4% on Day 28 (7.8 ± 9.3%). At the same time no changes in mass-specific respiratory capacities, mitochondrial protein or antioxidant content were found. This study demonstrates that skeletal muscle MitoVD may increase with 28 days acclimation to 3454 m. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    The Journal of Physiology 09/2015; DOI:10.1113/JP271118 · 5.04 Impact Factor
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    • "Animals living at high altitude have developed a certain adaptability which makes them more tolerant to hypoxic environments. These adaptive characteristics involve a variety of behavioral (Scott, 2011; Virués-Ortega et al., 2006), physiological (Monge and Leon-Velarde, 1991), biochemical (Scott, 2011; Weber, 2007) and genetic (Qiu et al., 2012; Storz et al., 2010) changes. Among the wide range of changes, the free radical metabolism has been an integral part of the metabolic depression machinery related to tolerance to hypoxia and anoxia (Hermes-Lima and Zenteno-Savın, 2002; Orr et al., 2009; Storey, 1996). "
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    ABSTRACT: Oxidative stress is a major challenge of survival for animals living on the plateau at different stages, however, lifelong exposure to high altitude could generate certain adaptability which makes them more tolerant to these environments. The aim of the present study was to compare the oxidative stress and antioxidant status between low altitude (LA, 2900m) and high altitude (HA, 4200m) populations of Phrynocephalus vlangalii. The results showed that the malondiadehyde levels in HA population decreased significantly in brain, but markedly increased in muscle and had no significant difference in liver compared to LA. The activity of catalase in brain was much higher in HA than LA. Except total antioxidant capacity and glutathione reductase, other antioxidants were similar between two populations in livers. By contrast, the levels of most antioxidants in muscle decreased markedly with elevation. We also explored the effects of hypoxia on oxidative damage and antioxidant defenses in P. vlangalii. The lizards were acclimated in simulated hypoxic chamber (15% O2 and 8% O2) for 6 weeks. The results showed that in 8% O2 group the levels of malondiadehyde, catalase, glutathione and total antioxidant capacity in brain and malondiadehyde, catalase and superoxide dismutase in liver were significantly higher than 15% O2 group. These findings indicate that in this species the oxidative stress and antioxidant capacity are subject to altitude and hypoxia and the lizards living at high altitude may have acquired some ability to deal with the oxidative stress. Copyright © 2015. Published by Elsevier Inc.
    Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 08/2015; 190. DOI:10.1016/j.cbpa.2015.08.013 · 1.97 Impact Factor
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    • "The concurrent declines in temperature and oxygen tension with elevation are a particular challenge to small highland mammals, which must sustain high rates of aerobic metabolism to support thermogenesis and locomotion in spite of a diminished oxygen supply (Hayes 1989). Both genotypic specialization and phenotypic plasticity in the physiological systems that mediate oxygen transport and utilization could be important for meeting this challenge in highland natives, but we are just beginning to understand the mechanisms involved (Storz, Scott, et al. 2010; Scott 2011; Cheviron and Brumfield 2012). "
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    ABSTRACT: At high-altitude, small mammals are faced with the energetic challenge of sustaining thermogenesis and aerobic exercise in spite of the reduced O2 availability. Under conditions of hypoxic cold stress, metabolic demands of shivering thermogenesis and locomotion may require enhancements in the oxidative capacity and O2 diffusion capacity of skeletal muscle to compensate for the diminished tissue O2 supply. We used common-garden experiments involving highland and lowland deer mice (Peromyscus maniculatus) to investigate the transcriptional underpinnings of genetically based population differences and plasticity in muscle phenotype. We tested highland and lowland mice that were sampled in their native environments as well as lab-raised F1 progeny of wild-caught mice. Experiments revealed that highland natives had consistently greater oxidative fiber density and capillarity in the gastrocnemius muscle. RNA sequencing analyses revealed population differences in transcript abundance for 68 genes that clustered into two discrete transcriptional modules, and a large suite of transcripts (589 genes) with plastic expression patterns that clustered into five modules. The expression of two transcriptional modules was correlated with the oxidative phenotype and capillarity of the muscle, and these phenotype-associated modules were enriched for genes involved in energy metabolism, muscle plasticity, vascular development, and cell stress response. Although most of the individual transcripts that were differentially expressed between populations were negatively correlated with muscle phenotype, several genes involved in energy metabolism (e.g., Ckmt1, Ehhadh, Acaa1a) and angiogenesis (Notch4) were more highly expressed in highlanders, and the regulators of mitochondrial biogenesis, PGC-1α (Ppargc1a) and mitochondrial transcription factor A (Tfam), were positively correlated with muscle oxidative phenotype. These results suggest that evolved population differences in the oxidative capacity and capillarity of skeletal muscle involved expression changes in a small suite of coregulated genes. © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: [email protected] /* */
    Molecular Biology and Evolution 04/2015; 32(8). DOI:10.1093/molbev/msv076 · 9.11 Impact Factor
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